Stromal infrastructure of the lymph node and coordination of immunity

Trends in Immunology

Volumn 36, Issue 1, 2015, Pages 30-39

  Chang, Jonathan E ^a,b   Turley, Shannon J ^c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN;

ADAPTIVE IMMUNITY; CELL FUNCTION; CELLULAR DISTRIBUTION; DENDRITIC CELL; HOMEOSTASIS; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; LYMPH NODE; LYMPHOCYTE; LYMPHOCYTE RECIRCULATION; NONHUMAN; REVIEW; STROMA CELL; ANIMAL; CELL MOTION; CYTOLOGY; HUMAN; IMMUNITY; IMMUNOLOGY; IMMUNOSURVEILLANCE; METABOLISM; PHYSIOLOGY;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS; CELL MOVEMENT; DENDRITIC CELLS; HOMEOSTASIS; HUMANS; IMMUNITY; IMMUNOLOGIC SURVEILLANCE; LYMPH NODES; LYMPHOCYTES; STROMAL CELLS;

EID: 84919835281     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2014.11.003     Document Type: Review

References (114)

1. Bleul C.C., et al. A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J. Exp. Med. 1996, 184:1101-1109.
2. Gunn M.D., et al. A B-cell-homing chemokine made in lymphoid follicles activates Burkitt's lymphoma receptor-1. Nature 1998, 391:799-803.
3. Gunn M.D., et al. A chemokine expressed in lymphoid high endothelial venules promotes the adhesion and chemotaxis of naive T lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:258-263.
4. Ngo V.N., et al. Epstein-Barr virus-induced molecule 1 ligand chemokine is expressed by dendritic cells in lymphoid tissues and strongly attracts naive T cells and activated B cells. J. Exp. Med. 1998, 188:181-191.
5. Forster R., et al. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 1999, 99:23-33.
6. Springer T.A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 1994, 76:301-314.
7. von Andrian U.H., et al. Homing and cellular traffic in lymph nodes. Nat. Rev. Immunol. 2003, 3:867-878.
8. Cyster J.G., et al. Sphingosine-1-phosphate and lymphocyte egress from lymphoid organs. Annu. Rev. Immunol. 2012, 30:69-94.
9. Mionnet C., et al. High endothelial venules as traffic control points maintaining lymphocyte population homeostasis in lymph nodes. Blood 2011, 118:6115-6122.
10. Bai Z., et al. Constitutive lymphocyte transmigration across the basal lamina of high endothelial venules is regulated by the autotaxin/lysophosphatidic acid axis. J. Immunol. 2013, 190:2036-2048.
11. Nakasaki T., et al. Involvement of the lysophosphatidic acid-generating enzyme autotaxin in lymphocyte-endothelial cell interactions. Am. J. Pathol. 2008, 173:1566-1576.
12. Moussion C., et al. Dendritic cells control lymphocyte entry to lymph nodes through high endothelial venules. Nature 2011, 479:542-546.
13. Onder L., et al. Endothelial cell-specific lymphotoxin-beta receptor signaling is critical for lymph node and high endothelial venule formation. J. Exp. Med. 2013, 210:465-473.
14. Herzog B.H., et al. Podoplanin maintains high endothelial venule integrity by interacting with platelet CLEC-2. Nature 2013, 502:105-109.
15. Grigorova I.L., et al. Lymph node cortical sinus organization and relationship to lymphocyte egress dynamics and antigen exposure. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:20447-20452.
16. Grigorova I.L., et al. Cortical sinus probing, S1P1-dependent entry and flow-based capture of egressing T cells. Nat. Immunol. 2009, 10:58-65.
17. Matloubian M., et al. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 2004, 427:355-360.
18. Pham T.H., et al. S1P1 receptor signaling overrides retention mediated by G alpha i-coupled receptors to promote T cell egress. Immunity 2008, 28:122-133.
19. Schwab S.R., et al. Lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science 2005, 309:1735-1739.
20. Pappu R., et al. Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine-1-phosphate. Science 2007, 316:295-298.
21. Pham T.H., et al. Lymphatic endothelial cell sphingosine kinase activity is required for lymphocyte egress and lymphatic patterning. J. Exp. Med. 2010, 207:17-27.
22. Lee M.J., et al. Sphingosine-1-phosphate as a ligand for the G protein-coupled receptor EDG-1. Science 1998, 279:1552-1555.
23. Lo C.G., et al. Cyclical modulation of sphingosine-1-phosphate receptor 1 surface expression during lymphocyte recirculation and relationship to lymphoid organ transit. J. Exp. Med. 2005, 201:291-301.
24. Tomura M., et al. Monitoring cellular movement in vivo with photoconvertible fluorescence protein 'Kaede' transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:10871-10876.
25. Hall J.G., et al. The immediate effect of antigens on the cell output of a lymph node. Br. J. Exp. Pathol. 1965, 46:450-454.
26. Baekkevold E.S., et al. The CCR7 ligand elc (CCL19) is transcytosed in high endothelial venules and mediates T cell recruitment. J. Exp. Med. 2001, 193:1105-1112.
27. Palframan R.T., et al. Inflammatory chemokine transport and presentation in HEV: a remote control mechanism for monocyte recruitment to lymph nodes in inflamed tissues. J. Exp. Med. 2001, 194:1361-1373.
28. Sixt M., et al. The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node. Immunity 2005, 22:19-29.
29. Shiow L.R., et al. CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 2006, 440:540-544.
30. Soderberg K.A., et al. Innate control of adaptive immunity via remodeling of lymph node feed arteriole. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:16315-16320.
31. Kumar V., et al. Optical projection tomography reveals dynamics of HEV growth after immunization with protein plus CFA and features shared with HEVs in acute autoinflammatory lymphadenopathy. Front. Immunol. 2012, 3:282.
32. Webster B., et al. Regulation of lymph node vascular growth by dendritic cells. J. Exp. Med. 2006, 203:1903-1913.
33. Chyou S., et al. Fibroblast-type reticular stromal cells regulate the lymph node vasculature. J. Immunol. 2008, 181:3887-3896.
34. + cells and then by T and B cells. J. Immunol. 2011, 187:5558-5567.
35. Kumar V., et al. Global lymphoid tissue remodeling during a viral infection is orchestrated by a B cell-lymphotoxin-dependent pathway. Blood 2010, 115:4725-4733.
36. Yang C.Y., et al. Trapping of naive lymphocytes triggers rapid growth and remodeling of the fibroblast network in reactive murine lymph nodes. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:E109-E118.
37. Acton S.E., et al. Dendritic cells control fibroblastic reticular network tension and lymph node expansion. Nature 2014, 514:498-502.
38. Astarita J.L., et al. The CLEC-2-podoplanin axis controls the contractility of fibroblastic reticular cells and lymph node microarchitecture. Nat. Immunol. 2014, Published online October 27, 2014. http://dx.doi.org/10.1038/ni.3035.
39. Kamath A.T., et al. Developmental kinetics and lifespan of dendritic cells in mouse lymphoid organs. Blood 2002, 100:1734-1741.
40. Steinman R.M. The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 1991, 9:271-296.
41. Baluk P., et al. Functionally specialized junctions between endothelial cells of lymphatic vessels. J. Exp. Med. 2007, 204:2349-2362.
42. Schmid-Schonbein G.W. Microlymphatics and lymph flow. Physiol. Rev. 1990, 70:987-1028.
43. von der Weid P.Y. Review article: lymphatic vessel pumping and inflammation - the role of spontaneous constrictions and underlying electrical pacemaker potentials. Aliment. Pharmacol. Ther. 2001, 15:1115-1129.
44. Acton S.E., et al. Podoplanin-rich stromal networks induce dendritic cell motility via activation of the C-type lectin receptor CLEC-2. Immunity 2012, 37:276-289.
45. Randolph G.J., et al. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat. Rev. Immunol. 2005, 5:617-628.
46. Teijeira A., et al. Taking the lymphatic route: dendritic cell migration to draining lymph nodes. Semin. Immunopathol. 2014, 36:261-274.
47. Schumann K., et al. Immobilized chemokine fields and soluble chemokine gradients cooperatively shape migration patterns of dendritic cells. Immunity 2010, 32:703-713.
48. Tal O., et al. DC mobilization from the skin requires docking to immobilized CCL21 on lymphatic endothelium and intralymphatic crawling. J. Exp. Med. 2011, 208:2141-2153.
49. Weber M., et al. Interstitial dendritic cell guidance by haptotactic chemokine gradients. Science 2013, 339:328-332.
50. Hoogewerf A.J., et al. Glycosaminoglycans mediate cell surface oligomerization of chemokines. Biochemistry 1997, 36:13570-13578.
51. Lee K.M., et al. D6 facilitates cellular migration and fluid flow to lymph nodes by suppressing lymphatic congestion. Blood 2011, 118:6220-6229.
52. Lee K.M., et al. D6: the 'crowd controller' at the immune gateway. Trends Immunol. 2013, 34:7-12.
53. de Paz J.L., et al. Profiling heparin-chemokine interactions using synthetic tools. ACS Chem. Biol. 2007, 2:735-744.
54. Ulvmar M.H., et al. The atypical chemokine receptor CCRL1 shapes functional CCL21 gradients in lymph nodes. Nat. Immunol. 2014, 15:623-630.
55. Heinzel K., et al. A silent chemokine receptor regulates steady-state leukocyte homing in vivo. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:8421-8426.
56. Ulvmar M.H., et al. Atypical chemokine receptors. Exp. Cell Res. 2011, 317:556-568.
57. Roozendaal R., et al. The conduit system of the lymph node. Int. Immunol. 2008, 20:1483-1487.
58. Roozendaal R., et al. Conduits mediate transport of low-molecular-weight antigen to lymph node follicles. Immunity 2009, 30:264-276.
59. Nossal G.J., et al. Antigens in immunity. XV. Ultrastructural features of antigen capture in primary and secondary lymphoid follicles. J. Exp. Med. 1968, 127:277-290.
60. Carrasco Y.R., et al. B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity 2007, 27:160-171.
61. Junt T., et al. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 2007, 450:110-114.
62. Phan T.G., et al. Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat. Immunol. 2007, 8:992-1000.
63. Drinker C.K., et al. The filtering capacity of lymph nodes. J. Exp. Med. 1934, 59:393-405.
64. Iannacone M., et al. Subcapsular sinus macrophages prevent CNS invasion on peripheral infection with a neurotropic virus. Nature 2010, 465:1079-1083.
65. Gonzalez S.F., et al. Capture of influenza by medullary dendritic cells via SIGN-R1 is essential for humoral immunity in draining lymph nodes. Nat. Immunol. 2010, 11:427-434.
66. Tamburini B.A., et al. Antigen capture and archiving by lymphatic endothelial cells following vaccination or viral infection. Nat. Commun. 2014, 5:3989.
67. Bajenoff M., et al. Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 2006, 25:989-1001.
68. Forster R., et al. A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen. Cell 1996, 87:1037-1047.
69. Cremasco V., et al. B cell homeostasis and follicle confines are governed by fibroblastic reticular cells. Nat. Immunol. 2014, 15:973-981.
70. + T cells. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:12139-12144.
71. Link A., et al. Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat. Immunol. 2007, 8:1255-1265.
72. + T cells and limiting reconstitution in HIV-1 and SIV infections through damage to the secondary lymphoid organ niche. Semin. Immunol. 2008, 20:181-186.
73. Zeng M., et al. Cumulative mechanisms of lymphoid tissue fibrosis and T cell depletion in HIV-1 and SIV infections. J. Clin. Invest. 2011, 121:998-1008.
74. Mionnet C., et al. Identification of a new stromal cell type involved in the regulation of inflamed B cell follicles. PLoS Biol. 2013, 11:e1001672.
75. Bannard O., et al. Germinal center centroblasts transition to a centrocyte phenotype according to a timed program and depend on the dark zone for effective selection. Immunity 2013, 39:912-924.
76. Cyster J.G., et al. Follicular stromal cells and lymphocyte homing to follicles. Immunol. Rev. 2000, 176:181-193.
77. Wang X., et al. Follicular dendritic cells help establish follicle identity and promote B cell retention in germinal centers. J. Exp. Med. 2011, 208:2497-2510.
78. Katakai T. Marginal reticular cells: a stromal subset directly descended from the lymphoid tissue organizer. Front. Immunol. 2012, 3:200.
79. Katakai T., et al. Organizer-like reticular stromal cell layer common to adult secondary lymphoid organs. J. Immunol. 2008, 181:6189-6200.
80. Jarjour M., et al. Fate mapping reveals origin and dynamics of lymph node follicular dendritic cells. J. Exp. Med. 2014, 211:1109-1122.
81. Chai Q., et al. Maturation of lymph node fibroblastic reticular cells from myofibroblastic precursors is critical for antiviral immunity. Immunity 2013, 38:1013-1024.
82. Benedict C.A., et al. Specific remodeling of splenic architecture by cytomegalovirus. PLoS Pathog. 2006, 2:e16.
83. Cadman E.T., et al. Alterations of splenic architecture in malaria are induced independently of Toll-like receptors 2, 4, and 9 or MyD88 and may affect antibody affinity. Infect. Immun. 2008, 76:3924-3931.
84. Glatman Zaretsky A., et al. Infection with Toxoplasma gondii alters lymphotoxin expression associated with changes in splenic architecture. Infect. Immun. 2012, 80:3602-3610.
85. + T cells and dendritic cells during infection with Toxoplasma gondii. PLoS Pathog. 2009, 5:e1000505.
86. Mueller S.N., et al. Regulation of homeostatic chemokine expression and cell trafficking during immune responses. Science 2007, 317:670-674.
87. Mueller S.N., et al. Viral targeting of fibroblastic reticular cells contributes to immunosuppression and persistence during chronic infection. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:15430-15435.
88. St John A.L., et al. Salmonella disrupts lymph node architecture by TLR4-mediated suppression of homeostatic chemokines. Nat. Med. 2009, 15:1259-1265.
89. Scandella E., et al. Restoration of lymphoid organ integrity through the interaction of lymphoid tissue-inducer cells with stroma of the T cell zone. Nat. Immunol. 2008, 9:667-675.
90. Katakai T., et al. A novel reticular stromal structure in lymph node cortex: an immuno-platform for interactions among dendritic cells, T cells and B cells. Int. Immunol. 2004, 16:1133-1142.
91. + T helper 1 cell differentiation. Immunity 2012, 37:1091-1103.
92. Woodruff M.C., et al. Trans-nodal migration of resident dendritic cells into medullary interfollicular regions initiates immunity to influenza vaccine. J. Exp. Med. 2014, 211:1611-1621.
93. van de Pavert S.A., et al. Chemokine CXCL13 is essential for lymph node initiation and is induced by retinoic acid and neuronal stimulation. Nat. Immunol. 2009, 10:1193-1199.
94. Benezech C., et al. Lymphotoxin-beta receptor signaling through NF-kappaB2-RelB pathway reprograms adipocyte precursors as lymph node stromal cells. Immunity 2012, 37:721-734.
95. Vondenhoff M.F., et al. LTbetaR signaling induces cytokine expression and up-regulates lymphangiogenic factors in lymph node anlagen. J. Immunol. 2009, 182:5439-5445.
96. Kim D., et al. Regulation of peripheral lymph node genesis by the tumor necrosis factor family member TRANCE. J. Exp. Med. 2000, 192:1467-1478.
97. Benezech C., et al. Ontogeny of stromal organizer cells during lymph node development. J. Immunol. 2010, 184:4521-4530.
98. Cupedo T., et al. Presumptive lymph node organizers are differentially represented in developing mesenteric and peripheral nodes. J. Immunol. 2004, 173:2968-2975.
99. van de Pavert S.A., et al. New insights into the development of lymphoid tissues. Nat. Rev. Immunol. 2010, 10:664-674.
100. Brendolan A., et al. Mesenchymal cell differentiation during lymph node organogenesis. Front. Immunol. 2012, 3:381.
101. Koning J.J., et al. Interdependence of stromal and immune cells for lymph node function. Trends Immunol. 2012, 33:264-270.
102. Suzuki-Inoue K., et al. A novel Syk-dependent mechanism of platelet activation by the C-type lectin receptor CLEC-2. Blood 2006, 107:542-549.
103. Sancho D., et al. Signaling by myeloid C-type lectin receptors in immunity and homeostasis. Annu. Rev. Immunol. 2012, 30:491-529.
104. Colonna M., et al. Molecular characterization of two novel C-type lectin-like receptors, one of which is selectively expressed in human dendritic cells. Eur. J. Immunol. 2000, 30:697-704.
105. Astarita J.L., et al. Podoplanin: emerging functions in development, the immune system, and cancer. Front. Immunol. 2012, 3:283.
106. Malhotra D., et al. Transcriptional profiling of stroma from inflamed and resting lymph nodes defines immunological hallmarks. Nat. Immunol. 2012, 13:499-510.
107. Martin-Villar E., et al. Podoplanin binds ERM proteins to activate RhoA and promote epithelial-mesenchymal transition. J. Cell Sci. 2006, 119:4541-4553.
108. Suzuki-Inoue K., et al. Essential in vivo roles of the C-type lectin receptor CLEC-2: embryonic/neonatal lethality of CLEC-2-deficient mice by blood/lymphatic misconnections and impaired thrombus formation of CLEC-2-deficient platelets. J. Biol. Chem. 2010, 285:24494-24507.
109. Osada M., et al. Platelet activation receptor CLEC-2 regulates blood/lymphatic vessel separation by inhibiting proliferation, migration, and tube formation of lymphatic endothelial cells. J. Biol. Chem. 2012, 287:22241-22252.
110. Navarro A., et al. T1alpha/podoplanin is essential for capillary morphogenesis in lymphatic endothelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 295:L543-L551.
111. Benezech C., et al. CLEC-2 is required for development and maintenance of lymph nodes. Blood 2014, 123:3200-3207.
112. Douglas Y.L., et al. Pulmonary vein, dorsal atrial wall and atrial septum abnormalities in podoplanin knockout mice with disturbed posterior heart field contribution. Pediatr. Res. 2009, 65:27-32.
113. Ramirez M.I., et al. T1alpha, a lung type I cell differentiation gene, is required for normal lung cell proliferation and alveolus formation at birth. Dev. Biol. 2003, 256:61-72.
114. Peters A., et al. Th17 cells induce ectopic lymphoid follicles in central nervous system tissue inflammation. Immunity 2011, 35:986-996.